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An Integrated Multi-Omics Analysis of the NK603 Roundup-Tolerant GM

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An Integrated Multi-Omics Analysis of the NK603 Roundup-Tolerant GM www.nature.com/scientificreports OPEN An integrated multi-omics analysis of the NK603 Roundup-tolerant GM maize reveals metabolism Received: 17 August 2016 Accepted: 02 November 2016 disturbances caused by the Published: 19 December 2016 transformation process Robin Mesnage1,*, Sarah Z. Agapito-Tenfen2,*, Vinicius Vilperte3, George Renney4, Malcolm Ward4, Gilles-Eric Séralini5, Rubens O. Nodari3 & Michael N. Antoniou1 Glyphosate tolerant genetically modified (GM) maize NK603 was assessed as ‘substantially equivalent’ to its isogenic counterpart by a nutrient composition analysis in order to be granted market approval. We have applied contemporary in depth molecular profiling methods of NK603 maize kernels (sprayed or unsprayed with Roundup) and the isogenic corn to reassess its substantial equivalence status. Proteome profiles of the maize kernels revealed alterations in the levels of enzymes of glycolysis and TCA cycle pathways, which were reflective of an imbalance in energy metabolism. Changes in proteins and metabolites of glutathione metabolism were indicative of increased oxidative stress. The most pronounced metabolome differences between NK603 and its isogenic counterpart consisted of an increase in polyamines including N-acetyl-cadaverine (2.9-fold), N-acetylputrescine (1.8-fold), putrescine (2.7-fold) and cadaverine (28-fold), which depending on context can be either protective or a cause of toxicity. Our molecular profiling results show that NK603 and its isogenic control are not substantially equivalent. The application of genetic engineering (GE) to modify edible crops is often advocated as one of the most impor- tant scientific advances to improve farming systems and feed the world in a more sustainable manner1. GE has been used to create crops adapted to abiotic stress, resistant to pathogens, with a longer shelf life, or with enhanced nutritional properties. However, commercialization of these traits is currently minor. Agricultural genetically modified (GM) crops are dominated by plants engineered to tolerate application of a herbicide or/and to produce their own insecticides2. A total of 180 million hectares of GM crops are currently cultivated worldwide on around 1.5 billion hectares constituting approximately 10% of global arable land3. Approximately 80% of GM crops have been modified to tolerate application of and thus accumulate glyphosate-based herbicide residues without dying in order to facilitate weed management. Regulations for the release of genetically modified organisms (GMOs) of any kind in a country are covered by the national biosafety regulations of that nation. Guidance on risk assessment (RA) aim at identifying and avoiding adverse effects by early detection and proper evaluation of intended and potential unintended changes in a GMO. These should be detected and identified at early stages of RA, often referred to as “hazard identifi- cation”. Hazard identification is essential to the RA process as it sets the foundation of what is considered or observed in later steps in the risk assessment process4. In the US, the Food and Drug Administration considers 1Gene Expression and Therapy Group, King’s College London, Faculty of Life Sciences & Medicine, Department of Medical and Molecular Genetics, 8th Floor, Tower Wing, Guy’s Hospital, Great Maze Pond, London SE1 9RT, United Kingdom. 2Genøk, Center for Biosafety, The Science Park, P.O. Box 6418 Tromsø 9294, Norway. 3CropScience Department, Federal University of Santa Catarina, Rod. Admar Gonzaga 1346, 88034-000 Florianópolis, Brazil. 4Proteomics Facility, King’s College London, Institute of Psychiatry, London SE5 8AF, United Kingdom. 5University of Caen, Institute of Biology, EA 2608 and Network on Risks, Quality and Sustainable Environment, MRSH, Esplanade de la Paix, University of Caen, Caen 14032, Cedex, France. *These authors contributed equally to this work. Correspondence and requests for materials should be addressed to M.N.A. (email: [email protected]) SCIENTIFIC REPORTS | 6:37855 | DOI: 10.1038/srep37855 1 www.nature.com/scientificreports/ GM technology as an extension of conventional breeding and GMO crops are deregulated once nutritional and compositional “substantial equivalence” is demonstrated5. The set of parameters and analyses necessary to declare a GMO as substantially equivalent to its conventional counterpart is still vague and focuses on a restricted set of compositional variables, such as the amounts of protein, carbohydrate, vitamins and minerals. GMOs are then declared substantially equivalent when sufficient similarities appear for those selected variables6. Remarkably, while a majority of GMO crops have been modified to withstand and thus accumulate a herbicide without dying, analysis for residues for such pesticides are neglected in compositional assessment7. Recent technologies used to ascertain the molecular compositional profile of a system, such as transcriptom- ics, proteomics, metabolomics, epigenomics and mirnomics, collectively referred to as “omics technologies”, are used extensively in basic and applied science8. Comparative omics analyses have been performed comparing GMO crops and their isogenic counterpart. A number of them have shown metabolic disturbances from potential unintended effects of the GM transformation process in Bt maize9–12, glyphosate-tolerant soybean13–15, potato16, cotton17 and rice18. However, these studies do not report consistent or coherent results, which can be explained by the use of a variety of genetic backgrounds and/or different growth conditions, as well as variations in the technologies and threshold levels applied19. Indeed, the majority of authors of these types of studies conclude that the statistically significant changes observed between the conventional and the GM varieties are not bio- logically significant because they fall into the range of variations obtained in the comparisons between different conventionally-bred varieties, and under different environmental conditions11. However, other authors conclude that observed differences could reflect biologically significant, GM transformation process induced changes in protein profiles12 or metabolism20 when appropriate near-isogenic controls were applied and test crops grown at the same time and location to avoid differences brought about by variable environmental conditions20. Currently, no regulatory authority requires mandatory untargeted molecular profiling omics analysis to be performed but some acknowledge their potential relevance for food and feed derived from GM plants with specific metabolic pathways modified, or in situations where a suitable comparator is not available4,21. Despite being declared to be ‘substantially equivalent’, off target effects have been observed in non-target species for Bt toxin-producing GMO crops22–24. Additionally, laboratory animal feeding trials performed with some GM plants in comparison to the non-GM counterpart have been proposed to provide evidence of ill-health effects. Several laboratory studies consisting of 90-day feeding trials in rodents have been conducted to evaluate the safety of GMO crop consumption25,26. These investigations have frequently resulted in statistically significant differences in parameters reflective of disturbances in various organ systems and in particular liver and kidney biochemistry, but with interpretation of their biological significance, especially with respect to health implica- tions, being controversial27–29. Such differences in outcome in such laboratory animal feeding studies could have multiple sources including the presence of GMO-associated pesticide residues30,31. In an effort to provide insight into the substantial equivalence classification of a Roundup tolerant NK603 GM maize, we have performed proteomics and metabolomics analyses of NK603 (sprayed or unsprayed with Roundup) and isogenic maize kernels (Fig. 1). We used a TMT10plex isobaric mass tag labelling method and quantified proteins by Liquid chromatography-tandem mass spectrometry™ (LC-MS/MS). The metabolome profile was determined by ultrahigh performance liquid chromatography-tandem mass spectroscopy (UPLC-MS/MS). Altogether, our integrative analysis shows that the GM transformation process used to generate NK603 maize caused deep alterations in the proteome and metabolome profiles of this crop and results in marked metabolic changes. We conclude that NK603 maize is not compositionally equivalent to its non-GM isogenic counterpart as previously claimed. Results The objective of this investigation was to obtain a deeper understanding of the biology of the NK603 GM maize by molecular profiling (proteomics and metabolomics) in order to gain insight into its substantial equivalence classification. We began by undertaking an unsupervised exploratory analysis of variance structure. We integrated metabolome and proteome profiles of the NK603, cultivated either with or without Roundup, and its isogenic counterpart, into a two-step multiple co-inertia analysis (MCIA) process. First, a one-table ordination method transforms each multidimensional dataset (hyperspaces) separately into comparable lower dimensional spaces by finding axes maximizing the sum of the variances of the variables. The resulting variance structure can be described by a PCA (Additional file 3). The results show a clear separation of each feed type (NK603, NK603+ Roundup and control) in both platforms. Control samples had the most distinct proteome and metabolome pro- files as observed in PCA plots.
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